Motivation and the Control of Behaviour

We first came across the concept of the hierarchical structure of the brain, its organization in an ascending series of levels, in Chapter 9. Now, in this final chapter we look at the very highest levels of all, those that determine what we do rather than how we do it.

Actually, there is no very clear or logical distinction between ‘what’ and ‘how’ in this sense: the task of deciding what to do amounts in the end to deciding how to stay alive, or at worst, how to immortalize our genetic instructions. It is for this reason that the sensory inputs of this highest level come – paradoxically – not just from the special senses that tell us about the outside world, but also from interoceptive, self-monitoring senses that are usually considered so ‘low’ as to be beneath our conscious notice. What they provide is information about the physiological well-being of the body, the state of the milieu intérieur, and our distance from that final condition that awaits all of us.

Motivation

Why, in fact, do we ever bother to do anything at all?

The answer is basically to do with income and expenditure, of energy. Even at rest, we are remorselessly expending energy: if we don’t replace this energy, we die. If like corals or sea-anemones we were lucky enough to live in an environment where we were bombarded by food, we could just glue ourselves to rock and keep our mouths open. But for the big spenders, warm-blooded animals like us, the only way of keeping in surplus is to gamble. We expend a lot of energy as a stake, in order to perform actions from which we hope to get more in return, rather like a business investing some of its profit in the hope of even huger profits in the future. In a sense this decisionmaking – to do or not to do – is the most difficult task an organism has to undertake. As we shall see, the whole of the brain can usefully be thought of as a mechanism for reducing the risk, by making more and more accurate predictions about the likely result of any particular course of action, on the basis of past experience, stored not just in our brains, but in our books.

To put it another way, we need to apply the principles of homeostasis, which loom so large in general physiology, not just to the milieu intérieur but to the outside world as well. In addition to internal homeostasis, controlled by hormones and the autonomic nervous system (ANS), we have to add external homeostasis, controlled by the brain, achieved sometimes by literally altering our environment (wearing a pullover, for instance), but more often by moving to somewhere nicer, or by engulfing or penetrating things we like.

Motivational maps

But the decision process need not be as complex as this. In a simple creature – an amoeba is an extreme case – the nature of the fundamental mechanism is particularly obvious: its motivation is entirely a function of its immediate environment, sensed chemically: Consequently we see tropisms in response to gradients of things like food (positive) or poisons (negative). On the one hand, attractive stimuli set up a positive gradient down which the animal moves; on the other hand, threatening conditions create a negative gradient, and it moves away. So the amoeba’s environment is a sort of motivational potential field or contour map, and the amoeba is like a little charged particle that moves around in response to
local gradients, the path it traces out being a direct function of its environment. Very simple tropistic mechanisms like these give rise to surprisingly life-like behaviour, as in Dr Grey Walter’s pioneering electromechanical tortoise Elsie which ran amiably around the floor looking for light, or the interactive version in NeuroLab.

Though higher animals produce more complex behaviour, the mechanism is essentially the same. The added complexity comes about for two reasons.

First, because there are many more types of desirable and undesirable stimuli to which they may react, and many of them – perhaps most – are learnt: these are the secondary

motivators (like money) that through experience become associated with other more self-evidently desirable goals (Chapter 8, p. 177). Consequently each individual has its own classification of stimuli into desirable and undesirable categories, unique because it is the result of that individual’s own personal experience.

Second, because whether a particular stimulus like food is a motivator or not depends also on ones own need – in this case, whether or not one is hungry. Motivation, in other words, is something like the product of gradient and need, so changing patterns of need give rise to changing patterns of activity even though the environment itself is the same, and to an outsider the resulting behaviour may appear to be complex or even unpredictable. Thus Cambridge for me consists of a large number of separate gradient or contour maps, each corresponding to a different need: one for food, with high points at all the food shops and restaurants, one for money, centred on my bank and supplemented by cash machines, one for newspapers, one for avoiding rain, and so on. Which one is operative at any particular moment depends on my need at that moment, rather like those electrical maps sometimes seen at the more down-market tourist resorts, with bulbs that light up when you press one of a set of buttons marked ‘parking’, ‘pubs’, ‘post offices’ and so on.

So the fundamental limbic motivational computer has to be a sort of ‘yellow pages’ connecting particular needs with a kind of library of motivational maps of the outside world: like the tourist map, it translates information about need into the kind of tropistic data that can in turn be changed by the higher levels of the motor system into actual patterns of activity. Here A, B, C, etc. are separate needs such as hunger, thirst, etc., and each has its own stored motivational map that is activated in appropriate physiological circumstances. Some evidence suggests that these ‘yellow pages’ or motivational maps are embodied in the hippocampus. Hippocampal neurons have been found in the rat that respond specifically when the animal is at a particular point in its environment, for example within a maze that the rat has learnt; its involvement in certain kinds of learning was discussed in Chapter 13. In the example above, the shading represents average firing frequency of a unit in rat hippocampus at different points within an enclosure, showing that it seems to be
associated with a particular location. Similarly, brain scans of London-taxi drivers, who have to undergo a period of rigorous spatial learning, demonstrate an enlarged posterior hippocampus relative to matched controls.

Equally, it is the hypothalamus that provides information about need, about the state of the body, and projects to the hippocampus via the septal nuclei. It is the centre to which autonomic afferents project, and its neurons monitor such physiological states of the blood as glucose concentration, temperature and osmolarity, as well as levels of circulating hormones, that decides one’s state of need. It is also in the hypothalamus that primary consummatory responses such as eating and drinking may be triggered off by electrical stimulation. The hypothalamus is thus utterly at the heart of the neural mechanisms that generate motivation: it is discussed in detail later in this chapter (p. 278).

It is natural to feel a certain resistance to the notion that our own richly complex lives, the apparent wealth of choices open to us, and our sense of liberty to choose among them, could possibly be determined by so simple a mechanism. But as Herbert Simon has said, human behaviour is really rather simple, but because most people live in very complex physical, man-made and social environments, their actual behaviour appears extremely complicated; thus the path traced out by an ant moving over rough ground may be very complex in appearance, even though its behaviour is simply directed at getting back to its nest.

To some extent it is in fact possible to plot motivational maps in Man: by averaging over large numbers of individuals, it is not difficult to measure quite directly the same kinds of tropistic gradients for us humans, that work so well in describing what an amoeba does. If you take a group of people and ask them the very simple question ‘Where in Britain would you like to be?’, it is possible to obtain contour maps of average preferences, in this case of the relative desirability amongst a group of school-leavers of different parts of the country. These are certainly motivational maps, in the sense that if the individuals had the means to do it, they would be translated into actual migratory behaviour not very different in essence from our amoeba moving blindly down its tropistic gradient.

Emotion

But motivational tropisms are not the only kind of behaviour. Some of our activity is not aimed directly at achieving particular goals in the way that the tropisms are; instead it is preparatory to the directed behaviour itself. The release of adrenaline associated with the need for sudden exertion is a classic example: it has the obvious effect of preparing the muscles and circulatory system for action. This sort of thing is what is meant in the widest sense by emotional behaviour; the emotions that we may feel at the same time are the sensory side-effects of this undirected behaviour. There are as many types of emotional behaviour as there are types of motivational goal, and they include some kinds of activity that are not regarded as ‘emotional’ in common parlance. Salivation, for example, is in this sense an emotional response accompanying the directed behaviour of getting food and eating it; and penile erection is an obvious preparatory response to another kind of goal. Much of the release of hormones falls in this general category, as for example the surge of luteinizing hormone (LH) that triggers ovulation in response to copulation in some species. Thinking of emotion and emotional behaviour in this more inclusive way helps to dispel some of the misunderstanding and muddle that tend to surround this topic.

As Man has a richer set of possible needs and goals, including abstract or even spiritual ones, so his types of emotional behaviour and emotional sensations are more varied and complex. But there are two absolutely basic emotional patterns found throughout the animal kingdom, and perfectly evident in Man as well, associated with tropisms of any kind: these are arousal and conservation.

Two basic emotional states

Arousal signifies the emotional state associated with a steep tropistic gradient, which may be either towards a
desirable goal or away from a source of threat (p. 274): the state often described by physiologists as ‘fight, fright or flight’, that results in an increase in the general activity of the sympathetic system, and the release of adrenaline. The consequent bodily responses are all of more or less obvious use in preparing the body for the expenditure of the energy that will be used to achieve the goal: blood flow through the muscles is increased, the heart rate is raised, glucose is released into the blood, the bronchioles and pupils dilate, the electrical activity of the brain increases, reaction times get quicker, and there is an associated feeling of general excitement. All of this of course involves a certain expenditure of energy, and would be a drain on the body’s resources if kept up for a long time: but much is now at stake, and the gamble is one worth taking.

Conservation or withdrawal is in a sense the opposite of arousal. In a situation like the one above, when every possible action is unpleasant – like standing in the middle of a minefield – the only sensible response is to conserve one’s resources, and do nothing at all, in the hope that the difficulties will go away of their own accord. The result is inactivity and stupor, a loss of muscle tone, sleep or even hibernation; if the situation is a sudden one, there may be abrupt immobility or freezing – the animal thus incidentally making itself inconspicuous and feigning death (a common response to oncoming motor-cars, but not a particularly helpful one). By all these means the rate of energy expenditure is greatly reduced, enabling the animal to ride out what may be only a temporary state of siege. The associated feelings are of apathy, tiredness and weakness: because of the reduction in muscle tone, one may actually feel heavier, pressed to the ground – the origin of the word ‘depression’. Loss of muscle tone in the face produces a characteristic sagging of the lower jaw and of the corners of the mouth, and bowed head. In mild forms, the conservation state occurs only too commonly when a person feels that nothing is worth doing and circumstances are against him, giving rise to reactive depression. The more acute form of conservation is fortunately only rarely seen, except in response to cataclysmic disasters. The woman shown above has just emerged from shelter after an earthquake that has destroyed most of the town in which she lived. The objective signs of conservation are obvious: the stooped posture, the hand lifted to the face to support the dropped jaw, the immobile staring eyes. In such circumstances one may find a general state of apathy and inactivity that continues for a long time and is not conducive to survival. A curious feature of such chronic depression, though one that is readily understandable in terms of motivational maps, is that in times of severe and particular stress, as in war, the incidence of this kind of emotional state actually decreases, perhaps because collective activity is required. Sleep can usefully be regarded as a variety of conservation, but is considered in a separate section below (p. 288).

We seldom see either of these two kinds of emotional state in their pure forms. Real objects tend to be both attractive and repellent: a hunting animal’s prey may both be desirable as food and also dangerous, and in many species even the sexual act is a risky undertaking for the male. It can be illuminating to think of emotions in terms of a continuum of mixed types distributed around the two primary axes of arousal and conservation, emphasizing the ambivalent nature of such states as rage and fear, the knife-edge between attack and retreat. Food does not usually have quite this effect on humans – dining is
rarely a frightening experience in modern society – but rage can easily be elicited in situations of frustration, when the positive and negative aspects of a possible goal are nicely balanced. The nature of the goal clearly affects the precise response that is made, yet there can often be a curious generality about arousal, most obvious perhaps in human sexual behaviour: sexual aggression shades off imperceptibly into sadism, and affection is expressed by licking and biting and other responses more appropriate to an edible goal.

Neural mechanisms

Of course such schemes are over-simplistic; for one thing, they ignore the important part that memory, especially the kind of anticipatory memory discussed in Chapter 13, in connection with the frontal lobes, may play in introducing an extra temporal dimension into our emotions: such emotional states as hope, worry, confidence and regret clearly involve an element of this kind. But it may help us to remember that there is nothing particularly recherché or high-falutin’ about human emotional responses, and no reason to suppose that they are produced by fundamentally different mechanisms from those generating the remarkably similar patterns of behaviour seen in other animals.

In short, keeping alive is a matter of monitoring the milieu intérieur and making homeostatic adjustments to it, adjustments that are partly neural and autonomic and partly hormonal: internal responses to internal stimuli. But this process is made much more effective by reacting to external stimuli as well, and by generating external responses. The development of the brain has permitted more and more sophisticated analysis of external stimuli, and greater and greater elaboration of patterns of external response, so that most of its bulk is concerned either with sensory analysis or motor coordination. But in the end, the only part of it that really matters is the region where the four fundamental signals – internal and external inputs and outputs – actually come together. That region is the hypothalamus.

The hypothalamus

Control of the pituitary

The hypothalamus lies on either side of the third ventricle, immediately above the pituitary (hypophysis) and below the thalamus, and consists of several fairly distinct nuclei. At its lowest level, it controls the pituitary (hypophysis), through two distinct mechanisms: one is direct, the other indirect.

Direct: the axons of magnocellular neurons (black, p. 279) in the supraoptic and paraventricular nuclei pass right down into the pituitary stalk to terminate in the posterior lobe (neurohypophysis). Here they release their transmitters, not at synaptic junctions but directly into the bloodstream; thus these neurons are acting directly as endocrine cells, and their transmitters are actually hormones. Neurons of the supraoptic region predominantly release antidiuretic hormone (ADH), those of the paraventricular region mostly oxytocin. Both these hormones are nonapeptides of very similar structure, but their effects are entirely different. ADH helps control the osmolarity of the blood by stimulating the retention of water in the kidney; in large doses it may also increase blood pressure through arteriolar constriction (hence its alternative name of vasopressin). Oxytocin stimulates the smooth muscle of the uterus in labour, and also causes milk ejection during lactation; in both cases the stimulus to its release is essentially neural, predominantly from mechanoreceptors in the regions concerned.

Indirect: the other route by which the hypothalamus controls the secretion of hormones from the pituitary is quite different. Axons from other, parvocellular, hypothalamic neurons terminate in a region on the ventral surface (the median eminence) where a system of fenestrated capillaries carries arterial blood down to the anterior pituitary through a portal system. The substances released from their terminals (releasing or inhibiting hormones: black dots) enter this portal system and are transported to the anterior pituitary where they each either stimulate or inhibit the release of some corresponding pituitary hormone from endocrine cells (blue). Thus the release of the pituitary hormone prolactin, which stimulates the secretion of milk and has other functions related to pregnancy, is stimulated by prolactin-releasing hormone (PRH) and inhibited by prolactin-inhibiting hormone (PIH), from medial regions of the hypothalamus. Other hypothalamic hormones have their corresponding pituitary ones: apart from PIH (which is known to be dopamine) they are all small peptides.

Homeostatic functions

Though scarcely larger than a peanut, the hypothalamus has an absolutely fundamental role in the control of behaviour. The reason is that – uniquely – it straddles the blood and the brain. At its lowest level – as we have just seen – it directly oversees the endocrine mechanisms that dominate hormonal and metabolic functions. In
doing this it relies on the fact that it is itself capable of monitoring critical aspects of the blood, notably blood glucose, temperature and osmolarity: the hypothalamus is a death predictor. At an intermediate level it acts as what Sherrington called the head ganglion of the autonomic system, effectively being in charge of the whole of the milieu intérieur, through its autonomic efferents that control the heart, digestive tract and other vital organs. Again, it is able to do this effectively because it has feedback from the body through autonomic afferents. In both cases, sensory information about the internal state of the body – S_int – is used as feedback to create homeostatic internal responses – R_int. The intermingled coordination of these two kinds of feedback control – partly hormonal, partly neural – is what keeps us alive.

Table 14.1 Hypothalamic control of the pituitary

Pituitary hormone	Control of release	Actions
Oxytocin	Neural	Milk ejection Uterine contraction
Vasopressin (ADH)	Neural	Water retention Vasoconstriction
Growth hormone (GH)	GHRH, GHIH	Medium-term provision of metabolic energy Promotion of growth
Thyroid stimulating hormone (TSH)	Hypothalamic thyrotropin-releasing hormone (TRH)	Stimulates thyroid; its hormones raise body temperature and have other miscellaneous effects
Adrenocorticotropic hormone (ACTH)	Corticotropin-releasing hormone (CRH)	Regulates levels of cortisol and androgens from the adrenal cortex; some effects on aldosterone as well
Luteinizing hormone (LH)	LH releasing hormone (LHRH)	Stimulates ovulation or testosterone secretion
Follicle-stimulating hormone (FSH)	GRH	Stimulates follicular growth or spermatogenesis
Prolactin	PRH, PIH	Stimulates milk secretion and maternal behaviour
Melanocyte-stimulating hormone (MSH)	MSH releasing and inhibiting hormones (MRH, MIH)	Controls skin colour in some species; in Man, function unclear

In the course of evolution what was already a beautifully functioning system became dramatically better. Partly this was a matter of prediction: From the special senses, sensory cues about the outside world could be interpreted through experience to anticipate what was going to happen to the milieu intérieur – think of temperature receptors in the skin, for example, or information about general light level telling you about the time of day, or taste receptors telling you that you’re about to experience an elevation of blood glucose. Thus the internal sensory signals, S_int, came to be supplemented by external ones, S_ext. At the same time, on the output side, the hypothalamus developed the ability to generate actual behaviour – R_ext as well as R_int – through its projections to limbic and motor pathways: a sensible response to cold is putting more clothes on; a sensible
response to a river if you’re thirsty is to bend down and drink. The hypothalamus is both the ultimate detector of need, and the ultimate generator of behaviour: the rest of the brain is really just a way of making the hypothalamus work better.

It may be helpful to reinforce this fundamental point by examining a number of specific instances of homeostatic systems in which hormonal and neural signals are integrated by the hypothalamus to produce external, behavioural, responses as well as internal ones.

Hypothalamus and glucostasis

The control of blood glucose is a particularly clear example of the interplay between internal and external homeostasis. On the one hand, there are the well-known hormonal mechanisms that ensure that glucose flooding in from the gut during a meal is quickly stored away, and later distributed to longer-term depots; in addition, there are several hormonal mechanisms that liberate glucose from these stores, during acute or chronic periods of need. On the other hand, it is only through behaviour – predation and ingestion – that glucose or its precursors will ever arrive in the gut at all. And in the hypothalamus we find neurons that are concerned with all aspects of both internal and external glucostasis.

The ventromedial and lateral areas regulate feeding behaviour by monitoring the level of blood glucose, and this information is also used in a negative feedback loop that regulates pituitary growth hormone release by means of GHRH and GHIH (somatostatin) in response to fluctuations in blood glucose. The ventromedial hypothalamus has also long been known to be associated with the control of eating. An animal with a lesion in the ventromedial area develops a voracious appetite, as if unable to sense when it has had enough, and as a consequence it becomes obese. Lesions in the lateral hypothalamus have exactly the opposite effect: appetite is reduced, the animal displays little interest in food and loses weight. For this reason, the lateral area is often described as a ‘feeding centre’, and the ventromedial area as a ‘satiety centre’. Cells of the ventromedial area take up glucose at a particularly high rate; as a consequence, injections of the poisonous glucose derivative gold thioglucose cause specific localized lesions that result in hyperphagia. In addition, the short-term control of eating is of course also dependent on sensory information coming both internally from the digestive tract and externally from smell and taste. Thus we have here a clear example of a system in which internal information from both the blood and viscera is used in conjunction with external stimuli to produce an integrated response that is partly internal (the regulation of growth hormone, and also the production of saliva and other digestive secretions, and other autonomic effects) and partly external – the eating itself.

Hypothalamus and fluid balanc

e\\The control of the concentration and volume of the body fluids is equally clearly a matter of cooperation between internal and external mechanisms of homeostasis, between hormonal regulation and drinking behaviour, and is associated particularly with the supraoptic region. Certain cells in this region act as osmoreceptors, stimulating the release of ADH when the blood becomes too concentrated; autonomic afferents carrying information about blood volume from stretch receptors in the venous circulation also appear to contribute to the control of ADH by the hypothalamus. Other information that is relevant to the regulation of water balance comes from receptors in the subfornical region, just above the hypothalamus; they respond to the hormone angiotensin II that essentially signals a low average blood pressure, but are more concerned with the regulation of drinking than with the control of ADH. Again, autonomic afferents from the oesophagus and stomach are also believed to contribute to thirst and to the initiation and especially the termination of drinking: animals stop drinking long before their body fluids have yet become fully rehydrated – if they didn’t, they would drink far too much. The effects of hypothalamic lesions suggest that like eating, drinking is controlled by two opposed systems located in different areas. Lesions in the supraoptic region produce excessive drinking (polydipsia), while those in the lateral hypothalamus reduce drinking as well as eating; electrical stimulation of the lateral nuclei, on the contrary, causes an animal to take in enormous amounts of water. The fact that lateral lesions affect both eating and drinking, and in rats have more generalized effects on other kinds of directed behaviour, suggests either that it has in some sense a more global role in mediating motivation, or perhaps that it is a mosaic of sub-regions devoted to specific varieties of directed behaviour.

Hypothalamus and temperature regulation

Temperature regulation is another example of homeostasis achieved through a mixture of internal and external responses: autonomically, hormonally, and also
through overt behaviour such as curling up in the cold and seeking warmth (not to mention putting on or taking off one’s clothes). Once again, the input to this system is partly neural and partly humoral; afferent signals from somatosensory warm and cold receptors, and from cells in the anterior hypothalamus that themselves respond to the temperature of the blood. Temperature regulation appears to be represented rather diffusely in the hypothalamus. Electrical stimulation at many points can produce fragments of temperature-regulating activity such as shivering, piloerection, vasoconstriction and sweating. Broadly speaking, the anterior half is concerned with mechanisms for losing heat in a hot environment and the posterior half with conserving heat when it is cold. More generally, there is a tendency for sympathetic responses to be found in the posterior half and parasympathetic in the anterior half. The fact that none of these effects is sharply localized simply reflects the high degree of inter-relationship that exists between different homeostatic functions: a given response such as vasoconstriction may be caused by many diverse kinds of stimulus (fear, low temperature, low blood pressure), and will in turn have a disturbing effect on several different homeostatic systems. The thyroid-stimulating hormone is controlled by TRH, associated with more ventral parts of the hypothalamus. The thyroid hormones have many interrelated effects on metabolism and growth, which are not well understood. One of its functions appears to be to cause a general increase in metabolic rate, helping to maintain body temperature under conditions of chronic cold.

Hypothalamus and reproduction

The endless multiplication of examples can soon become wearisome, and in any case leads far outside the scope of this book; the remaining pituitary outputs will be only mentioned very briefly. The gonadotropic hormones LH and FSH, jointly controlled by a single releasing factor (gonadotrophin releasing hormone, GRH), together with the pituitary hormone prolactin are the means by which the brain influences the reproductive systems. What is particularly interesting about them is that gonadal steroids feed back on to receptors in the hypothalamus, not only influencing the production of the hormones themselves (and thus generating reproductive cycles) but also controlling sexual and maternal behaviour through its descending control of reticulospinal neurons. They also illustrate very clearly how an essentially hormonal control system can be influenced by a host of different types of stimuli from the special senses. One need only think of the effects of light on the timing of ovulation and breeding seasons, of the effect of skin and other kinds of stimulation on sexual arousal, of the influence of the sound or smell of offspring on maternal behaviour, of pheromones on ovulation and mating, and so on. Similarly, the effects of the various kinds of internal and external stimuli that constitute ‘stress’ on the secretion of ACTH, which regulates the secretion of corticosteroids from the adrenals and is controlled by CRH, are well known: ACTH is actually quite widely distributed in the brain, including the superior colliculus and substantia nigra and amygdala. In addition, there are the melanocyte-stimulating hormones, regulating the pigmentation of the skin in certain species and released from the interstitial part of the pituitary, that are controlled in a similar way by MRH and MIH, under the influence predominantly of visual stimulation. (See Table 14.1.) And finally, a hypothalamic function that is not exactly homeostatic is its involvement in registering the passage of time, and thus in turn controlling large-scale patterns of behaviour such as sleep, hibernation, and reproductive behaviour in animals where this has a seasonal basis. The suprachiasmatic nucleus, which receives input directly from the retina informing it about the time of day but also has intrinsic circadian clocks, appears to play an essential part in this: it is discussed further on p. 288.

Relation to limbic system

The ancient neural pathways to and from the hypothalamus are not well understood. In particular, although it is evident that the hypothalamus is indeed ‘the head ganglion of the autonomic system’, it has not been possible to identify conclusively by what routes its autonomic functions are mediated. Its connections with the limbic system are clearer: it receives afferents from the hippocampal region through a massive fibre bundle (the fornix), and is interconnected through the medial forebrain bundle with many parts of the limbic system including the amygdala, with orbitofrontal cortex, and with reticular formation (RF), including the areas controlling respiration and the cardiovascular system (see p. 204). The medial forebrain bundle also carries afferent olfactory information. Some hypothalamic nuclei – notably the supraoptic and paraventricular, project to extraordinarily diverse areas, including substantia nigra and the substantia gelatinosa of the dorsal horn. Corresponding to this diverse output, stimulation of many regions of the hypothalamus can give rise to fragments of emotional behaviour such as sweating, piloerection, freezing, sexual responses, and so on.

The amygdala

The amygdala (‘almond’ – from its shape) appears to be an important structure on the output side: it projects partly to the hypothalamus (generating autonomic and hormonal effects) and is also capable of generating actual behaviour by two routes to the motor system: to dorsomedial nucleus of the thalamus, which projects in turn to frontal cortex; and to the nucleus accumbens (ventral striatum) which projects to parts of basal ganglia, particularly globus pallidus and substantia nigra. It can be broken down into three major divisions (basolateral, cortical and centromedial), further subdivided into 10 or so nuclei. The projection from the centromedial region to
the hypothalamus through the medial forebrain bundle is particularly interesting, as its organization seems to correspond rather nicely with the two fundamental types of emotion described earlier in this chapter, conservation and arousal.

The lateral area projects directly to the ventromedial hypothalamus, and broadly speaking both seem to correspond with conservation, the horizontal axis of the diagram on p. 277. Stimulation in this region of the amygdala produces passivity, and even sleep or stupor. Lesions in the ventromedial hypothalamus, the ‘satiety centre’, produce over-eating and obesity; again, similar effects are produced in the lateral amygdala, but with a more general affective change as well, an increase in irritability and aggressiveness.
The dorsomedial area projects directly on to the lateral hypothalamus, and both regions seem, broadly speaking, to be concerned with arousal, the activation of a positive motivational drive. We have already seen that the lateral hypothalamus is associated with the initiation of eating and drinking behaviour, in the sense that lesions give rise to aphagia and adipsia; but they also produce a more general depression: dogs with lateral hypothalamic lesions are described as having a sad appearance, and are listless and somnolent. Lesions of the dorsomedial amygdala have similar effects, with perhaps more of the general, affective, component; stimulation in this region may produce hissing and growling and other signs of positive arousal.
Large bilateral lesions that include the amygdala create an animal in which tropistic behaviour is greatly exaggerated (the Klüver-Bucy syndrome): everything in the environment seems indiscriminately attractive, and such a monkey will compulsively examine and try to eat such things as the bars of its cage and its own faeces, and even things like snakes that would terrify a normal animal. The same kind of hypertropism is seen in its sexual activity: the animal is markedly hypersexual and may try to copulate with members of its own sex, as well as inanimate objects. Again, it is as if objects do not receive their normal emotional colouring, and inappropriately directed behaviour results, though a complicating factor is that such widespread lesions also damage regions of temporal cortex involved more generally in visual recognition. Studies in humans have confirmed the general sense that the amygdala is in part involved in fear, aversion from stimuli that have been experienced as harmful. Early studies showed that electrical stimulation of the amygdala in conscious patients (as part of preliminary investigations of possible sites of epileptic disturbances) elicited feelings of fear, and lesions in this area are reported to interfere with the formation of associations with unpleasant stimuli. Some other studies suggest that the amygdala is concerned not just with aversive responses but also with positive responses to stimuli associated with reward.

More specifically sexual responses (as well as more general items of emotional expression such as pupil dilatation or changes in facial expression, and also respiratory responses) may be elicited from the cingulate gyrus, a primitive mesocortical region of the limbic system that receives a projection from the hypothalamus by way of the mammillary bodies and anterior thalamus, as well as from neocortex. Together with the nucleus accumbens, which appears to provide a link from the amygdala to the basal ganglia, it may provide another route by which the hypothalamus generates overt behaviour, though the functions of the cingulate remain unclear. Other regions of the limbic system are described as pleasure centres, in the sense that if an electrode is implanted in, for instance, the septal nuclei, and connected up so that when an animal presses a lever in its cage it receives a pulse of electrical stimulation through the electrode, then as soon as the animal discovers what the lever does, it will go on pressing it repeatedly, often in preference to ‘really’ pleasant stimuli such as food or sex. Of course one cannot tell whether it is feeling pleasure as a result: but it is clear that the electrode must in a sense be bypassing the normal motivational mechanisms of the hypothalamus and in some way activating the tropistic input to the motor system directly. Other sites that have been found to produce direct motivation of this kind include parts of the amygdala and the hypothalamus itself. In some locations (dorsomedial thalamus, amygdala, hypothalamus) electrical stimulation has exactly the opposite effect: once the lever is pressed, it is never pressed again, presumably because the stimulus is evoking avoidance rather than positive tropism; but one has to be sure in such cases that the animal is not merely feeling pain.

Decision

At the beginning of this chapter it was pointed out that the whole purpose of the evolutionary development of the brain is to help the hypothalamus in carrying out homeostasis, by making predictions: predictions about what we are about to experience, predictions about what
will be the result of doing this rather than that. If the world behaved with clockwork regularity, and if we had unlimited information about it, making decisions about how to respond to a particular stimulus would be entirely trivial, like playing noughts-and-crosses. But that is not the case; and just as a successful business makes the best estimates of the risks and potential gains from taking one course of action rather than another, so that its gambles tend to pay off, so the neural mechanisms that determine what we do must similarly compute the probabilities of different outcomes, and the rewards likely to accrue from different actions. The rational way to proceed is to calculate, over all the things we might do, the one for which the expected return (the size of the reward multiplied by the probability of getting it) is maximum. This would be relatively straightforward, if our sensory systems were fast, reliable and capacious: but they are not. As we have seen again and again, they are subject to noise (some originating in the outside world, some internally), and – by computer standards – operate with a very low bandwidth. The result, as has been repeatedly emphasized, is that we are continually making guesses about what’s going on, based mostly on our experience of what has happened in the past (embodied in our internal models) and only partly on real information trickling in through our senses (p. 255). The situation is not entirely unlike making a clinical diagnosis: on the one hand, the doctor has a lifetime’s experience of the probability of different kinds of disease, and this is supplemented by the often rather meagre information afforded by the patient in front of them. The question then arises, how to combine these two kinds of information – actual evidence and prior expectation – in order to arrive at the most likely assessment of the underlying cause.

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